Multigene, genus-wide phylogenetic studies have uncovered the limited taxonomic resolution power of commonly used gene markers, particularly of rRNA genes, to discriminate closely related species of the nematode genus Heterorhabditis. In addition, conflicting tree topologies are often obtained using the different gene markers, which limits our understanding of the phylo- and co-phylogenetic relationships and biogeography of the entomopathogenic nematode genus Heterorhabditis. Here we carried out phylogenomic reconstructions using whole nuclear and mitochondrial genomes, and whole ribosomal operon sequences, as well as multiple phylogenetic reconstructions using various single nuclear and mitochondrial genes. Using the inferred phylogenies, we then investigated co-phylogenetic relationships between Heterorhabditis and their Photorhabdus bacterial symbionts and biogeographical patterns. Robust, well-resolved, and highly congruent phylogenetic relationships were reconstructed using both whole nuclear and mitochondrial genomes. Similarly, whole ribosomal operon sequences proved valuable for phylogenomic reconstructions, though they have limited value to discriminate closely related species. In addition, two mitochondrial genes, the cytochrome c oxidase subunit I (cox-1) and the NADH dehydrogenase subunit 4 (nad-4), and two housekeeping genes, the fanconi-associated nuclease 1 (fan-1) and the serine/threonine-protein phosphatase 4 regulatory subunit 1 (ppfr-1), provided the most robust phylogenetic reconstructions compared to other individual genes. According to our findings, whole nuclear and/or mitochondrial genomes are strongly recommended for reconstructing phylogenetic relationships of the genus Heterorhabditis. If whole nuclear and/or mitochondrial genomes are unavailable, a combination of nuclear and mitochondrial genes can be used as an alternative. Under these circumstances, sequences of multiple conspecific isolates in a genus-wide phylogenetic context should be analyzed to avoid artefactual species over-splitting driven by the high intraspecific sequence divergence of mitochondrial genes and to avoid artefactual species lumping driven by the low interspecific sequence divergence of some nuclear genes. On the other hand, we observed that the genera Heterorhabditis and Photorhabdus exhibit diverse biogeographic patterns, ranging from cosmopolitan species to potentially endemic species, and show high phylogenetic congruence, although host switches have also occurred. Our study contributes to a better understanding of the biodiversity and phylo- and co-phylogenetic relationships of an important group of biological control agents and advances our efforts to develop more tools that are compatible with sustainable and eco-friendly agricultural practices.

Departamento de Sanidad Vegetal Facultad de Ciencias Agronómicas Universidad de Chile 8820808 Santiago Chile

Department of Conservation Ecology and Entomology Stellenbosch University Private Bag X1 7602 Matieland South Africa

Department of Plant Protection School of Agriculture Ferdowsi University of Mashhad 9177948978 Mashhad Iran

Department of Zoology Pachhunga University College 796001 Aizawl Mizoram India

Experimental Biology Research Group Institute of Biology University of Neuchâtel 2000 Neuchâtel Switzerland

Experimental Biology Research Group Institute of Biology University of Neuchâtel 2000 Neuchâtel Switzerland; Department of Biosciences University Center for Research and Development Chandigarh University 140413 Gharuan India

Institute of Entomology Biology Centre of the Czech Academy of Sciences CAS 37005 České Budějovice Czech Republic; Faculty of Agriculture and Technology University of South Bohemia 37005 České Budějovice Czech Republic

Laboratory of Diagnosis and Integrated Management of Plant Bio Aggressors University of Parakou BP123 Parakou Borgou Benin

Laboratory of Nematology Institute of Agrifood Animal and Environmental Sciences Universidad de O Higgins Chile

University of Florida IFAS Citrus Research and Education Center 33850 Lake Alfred Florida USA

USDA ARS SE Fruit and Tree Nut Research Laboratory 31008 Byron GA USA

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Description of Heterorhabditis americana n. sp. (Rhabditida, Heterorhabditidae), a new entomopathogenic nematode species isolated in North America